Aquatic Sciences

, Volume 72, Issue 2, pp 165–178 | Cite as

Fishing effects on age and spatial structures undermine population stability of fishes

  • Chih-hao HsiehEmail author
  • Atsushi Yamauchi
  • Takefumi Nakazawa
  • Wei-Fen Wang


Overfishing has caused dramatic changes in structures of exploited populations as well as ecosystems. In this article, we focus on fishing effects on age (size) and spatial structures of exploited fishes. Accumulating evidence has shown that large and experienced spawning individuals are able to produce higher quality and quantity of eggs, known as maternal effects, and that individuals of different age classes tend to spawn in different locations and times. These behaviors are associated with a healthy age structure and contribute to bet-hedging capacity that is important in smoothing out short-term environmental variability. Here, we document a widespread phenomenon of age (size)-truncation of exploited populations driven by size-selective fishery removals. Such size-selective fishing may have evolutionary consequence and may be difficult to reverse. In addition, fishing often reduces population spatial heterogeneity that also contributes importantly to bet-hedging. We review studies showing that the effects of age truncation and reduction of spatial heterogeneity have reduced resilience and elevated the fluctuation amplitude of exploited populations facing a changing environment. Recent analyses indicated that fish populations often exhibit nonlinear nature and have potential to shift dramatically in a short time. All the evidence suggests that fishing, by altering age or spatial structures, may make exploited fishes, more prone to catastrophic shifts. Therefore, to achieve sustainable fisheries, management should conserve the age and spatial structure in addition to viable spawning biomass.


Age (size) composition Spatial heterogeneity Maternal effects Bet-hedging Fisheries management Nonlinear catastrophic shifts 



This work is supported by NSC to CH and WW, the postdoctoral fellowship from NTU and JSPS to TN, and JSTA and the Global COE Program A06, Kyoto University to AY.

Supplementary material

27_2009_122_MOESM1_ESM.pdf (78 kb)
Appendixes 1 and 2 (PDF 77 kb)


  1. Aguilar-Perera A, Aguilar-Davila W (1996) A spawning aggregation of Nassau grouper Epinephelus striatus (Pisces: Serranidae) in the Mexican Caribbean. Environ Biol Fish 45:351–361CrossRefGoogle Scholar
  2. Andersen KH, Brander K (2009) Expected rate of fisheries-induced evolution is slow. Proc Natl Acad Sci 106:11657–11660CrossRefPubMedGoogle Scholar
  3. Anderson CNK, Hsieh CH, Sandin SA, Hewitt R, Hollowed A, Beddington J, May RM, Sugihara G (2008) Why fishing magnifies fluctuations in fish abundance. Nature 452:835–839CrossRefPubMedGoogle Scholar
  4. Bell JD, Lyle JM, Bulman CM, Graham KJ, Newton GM, Smith DC (1992) Spatial variation in reproduction, and occurrence of non-reproductive adults, in orange roughy, Hoplostethus atlanticus Collett (Trachichthyidae), from south-eastern Australia. J Fish Biol 40:107–122CrossRefGoogle Scholar
  5. Berkeley SA, Chapman C, Sograd SM (2004a) Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology 85:1258–1264CrossRefGoogle Scholar
  6. Berkeley SA, Hixon MA, Larson RJ, Love MS (2004b) Fisheries sustainability via protection of age structure and spatial distribution of fish populations. Fisheries 29:23–32CrossRefGoogle Scholar
  7. Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105Google Scholar
  8. Blanchard JL, Mills C, Jennings S, Fox CJ, Packham BD, Eastwood PD, O’Brien CM (2005) Distribution–abundance relationships for North Sea Atlantic cod (Gadus morhua): observation versus theory. Can J Fish Aquat Sci 62:2001–2009CrossRefGoogle Scholar
  9. Botsford LW, Castilla JC, Peterson CH (1997) The management of fisheries and marine ecosystems. Science 277:509–515CrossRefGoogle Scholar
  10. Browman HI, Stergiou KI (2004) Perspectives on ecosystem-based approaches to the management of marine resources. Mar Ecol Prog Ser 274:269–303CrossRefGoogle Scholar
  11. Cole L (1954) The population consequences of life history phenomena. Q Rev Biol 29:103–137CrossRefPubMedGoogle Scholar
  12. Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297:94–96CrossRefPubMedGoogle Scholar
  13. Daan N, Christensen V, Cury PM (2005) Quantitative ecosystem indicators for fisheries management. ICES J Mar Sci 62:307–614CrossRefGoogle Scholar
  14. Deevey ES Jr (1947) Life tables for natural populations of animals. Q Rev Biol 22:283–314CrossRefPubMedGoogle Scholar
  15. Dieckmann U, Heino M (2007) REVIEW: Probabilistic maturation reaction norms: their history, strengths, and limitations. Mar Ecol Prog Ser 335:253–269CrossRefGoogle Scholar
  16. Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat Sci 1:54–75CrossRefGoogle Scholar
  17. Engelhard GH, Heino M (2004) Maturity changes in Norwegian spring-spawning herring before, during, and after a major population collapse. Fish Res 66:299–310CrossRefGoogle Scholar
  18. FAO (2008) The state of world fisheries and aquaculture. RomeGoogle Scholar
  19. Field JG, Moloney CL, du Buisson L, Jarre A, Stroemme T, Lipinski MR, Kainge P (2008) Exploring the BOFFFF hypothesis using a model of southern African deepwater hake (Merluccius paradoxus). In: Tsukamoto K, Kawamura T, Takeuchi T, Beard JTD, Kaiser MJ (eds) Fisheries for global welfare and environment. Terrapub, Tokyo, pp 17–26Google Scholar
  20. Fisher JAD, Frank KT (2004) Abundance-distribution relationships and conservation of exploited marine fishes. Mar Ecol Prog Ser 279:201–213CrossRefGoogle Scholar
  21. Francis RC, Hixon MA, Clarke ME, Murawski SA, Ralston S (2007) Fisheries management: ten commandments for ecosystem-based fisheries scientists. Fisheries 32:217–233CrossRefGoogle Scholar
  22. Froese R, Stern-Pirlot A, Winker H, Gascuel D (2008) Size matters: how single-species management can contribute to ecosystem-based fisheries management. Fish Res 92:231–241CrossRefGoogle Scholar
  23. Fulton EA, Smith ADM, Punt AE (2005) Which ecological indicators can robustly detect effects of fishing? ICES J Mar Sci 62:540–551CrossRefGoogle Scholar
  24. Garcia SM, Zerbi A, Aliaume C, Do Chi T, Lasserre G (2003) The ecosystem approach to fisheries: issues, terminology, principles, institutional foundations, implementation and outlook. FAO Fish Tech Pap 443:1–71Google Scholar
  25. Gunderson LH, Vetter RD (2006) Temperate rocky reef fish. In: Kritzer JP, Sale PF (eds) Marine metapopulations. Elsevier, Amsterdam, pp 69–118CrossRefGoogle Scholar
  26. Heino M (1998) Management of evolving fish stocks. Can J Fish Aquat Sci 55:1971–1982CrossRefGoogle Scholar
  27. Heino M, Godo OR (2002) Fisheries-induced selection pressures in the context of sustainable fisheries. Bull Mar Sci 70:639–656Google Scholar
  28. Hilborn R (2004) Ecosystem-based fisheries management: the carrot or the stick? Mar Ecol Prog Ser 274:275–278Google Scholar
  29. Hsieh CH (2006) Separating environmental effects from fishing impacts on the dynamics of fish populations in the Southern California region. University of California, San DiegoGoogle Scholar
  30. Hsieh CH, Ohman MD (2006) Biological responses to environmental forcing: the linear tracking window hypothesis. Ecology 87:1932–1938CrossRefPubMedGoogle Scholar
  31. Hsieh CH, Glaser SM, Lucas AJ, Sugihara G (2005a) Distinguishing random environmental fluctuations from ecological catastrophes for the North Pacific Ocean. Nature 435:336–340CrossRefPubMedGoogle Scholar
  32. Hsieh CH, Reiss C, Watson W, Allen MJ, Hunter JR, Lea RN, Rosenblatt RH, Smith PE, Sugihara G (2005b) A comparison of long-term trends and variability in populations of larvae of exploited and unexploited fishes in the Southern California region: a community approach. Prog Oceanogr 67:160–185CrossRefGoogle Scholar
  33. Hsieh CH, Reiss CS, Hunter JR, Beddington JR, May RM, Sugihara G (2006) Fishing elevates variability in the abundance of exploited species. Nature 443:859–862CrossRefPubMedGoogle Scholar
  34. Hsieh CH, Anderson C, Sugihara G (2008a) Extending nonlinear analysis to short ecological time series. Am Nat 171:71–80CrossRefPubMedGoogle Scholar
  35. Hsieh CH, Reiss SC, Hewitt RP, Sugihara G (2008b) Spatial analysis shows fishing enhances the climatic sensitivity of marine fishes. Can J Fish Aquat Sci 65:947–961CrossRefGoogle Scholar
  36. Hsieh CH, Chen CS, Chiu TS, Lee KT, Shieh FJ, Pan J-Y, Lee MA (2009) Time series analyses reveal transient relationships between abundance of larval anchovy and environmental variables in the coastal waters southwest of Taiwan. Fish Oceanogr 18:102–117CrossRefGoogle Scholar
  37. Hutchings JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 13:297–309CrossRefGoogle Scholar
  38. ICCAT-SCRS (2006) Stock status report-Swordfish, North Atlantic, 2006. FAO, RomeGoogle Scholar
  39. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes P, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638CrossRefPubMedGoogle Scholar
  40. Jacobson LD, De Oliveira JAA, Barange M, Cisneros-Mata MA, Felix-Uraga R, Hunter JR, Kim JY, Matsuura Y, Niquen M, Porteiro C, Rothschild B, Sanchez RP, Serra R, Uriarte A, Wada T (2001) Surplus production, variability, and climate change in the great sardine and anchovy fisheries. Can J Fish Aquat Sci 58:1891–1903CrossRefGoogle Scholar
  41. Jennings S, Dulvy NK (2005) Reference points and reference directions for size-based indicators of community structure. ICES J Mar Sci 62:397–404CrossRefGoogle Scholar
  42. Jennings S, Kaiser Mj (1998) The effects of fishing on marine ecosystems. Adv Mar Biol 34:201–351CrossRefGoogle Scholar
  43. Jorgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K, Ernande B, Gardmark A, Johnston F, Matsumura S, Pardoe H, Raab K, Silva A, Vainikka A, Dieckmann U, Heino M, Rijnsdorp AD (2007) Managing evolving fish stocks. Science 318:1247–1248CrossRefPubMedGoogle Scholar
  44. Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish Fish 5:131–140Google Scholar
  45. Kuparinen A, Merila J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659CrossRefPubMedGoogle Scholar
  46. Laikre L, Palm S, Ryman N (2005) Genetic population structure of fishes: implications for coastal zone management. Ambio 34:111–119PubMedGoogle Scholar
  47. Law R (2007) Fisheries-induced evolution: present status and future directions. Mar Ecol Prog Ser 335:271–277CrossRefGoogle Scholar
  48. Law R, Grey DR (1989) Evolution of yields from populations with age-specific cropping. Evol Ecol 3:343–359CrossRefGoogle Scholar
  49. Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull Entomol Soc Am 15:237–240Google Scholar
  50. Levins R (1970) Extinction. In: Gesternhaber G (ed) Some mathematical problems in biology. Am Math Soc, Providence, pp 77–107Google Scholar
  51. Longhurst A (2002) Murphy’s law revisited: longevity as a factor in recruitment to fish populations. Fish Res 56:125–131CrossRefGoogle Scholar
  52. MacCall AD (1990) Dynamic geography of marine fish populations. University of Washington, WashingtonGoogle Scholar
  53. Marshall CT, Frank KT (1995) Density-dependent habitat selection by juvenile haddock (Melanogrammus aeglefinus) on the southwestern Scotian Shelf. Can J Fish Aquat Sci 52:1007–1017CrossRefGoogle Scholar
  54. Marshall CT, McAdam BJ (2007) Integrated perspectives on genetic and environmental effects on maturation can reduce potential for errors of inference. Mar Ecol Prog Ser 335:301–310CrossRefGoogle Scholar
  55. Marteinsdottir G, Gunnarsson B, Suthers IM (2000) Spatial variation in hatch date distributions and origin of pelagic juvenile cod in Icelandic waters. ICES J Mar Sci 57:1182–1195CrossRefGoogle Scholar
  56. McFarlane GA, Smith PE, Baumgartner TR, Hunter JR (2002) Climate variability and Pacific sardine populations and fisheries. Am Fish Soc Symp 32:195–214Google Scholar
  57. McQuinn IH (1997) Metapopulations and the Atlantic herring. Rev Fish Biol Fish 7:297–329CrossRefGoogle Scholar
  58. Morita K, Fukuwaka MA (2007) Why age and size at maturity have changed in Pacific salmon. Mar Ecol Prog Ser 335:289–294CrossRefGoogle Scholar
  59. Murawski SA, Rago PJ, Trippel EA (2001) Impacts of demographic variation in spawning characteristics on reference points for fishery management. ICES J Mar Sci 58:1002–1014CrossRefGoogle Scholar
  60. Murphy GI (1967) Vital statistics of the Pacific sardine (Sardinops caerulea) and the population consequences. Ecology 48:731–736CrossRefGoogle Scholar
  61. Murphy GI (1968) Pattern in life history and the environment. Am Nat 102:391–403CrossRefGoogle Scholar
  62. Nash RDM, Witthames PR, Pawson M, Alesworth E (2000) Regional variability in the dynamics of reproduction and growth of Irish Sea plaice, Pleuronectes platessa L. J Sea Res 44:55–64CrossRefGoogle Scholar
  63. O’Farrell MR, Botsford LW (2006a) Estimating the status of nearshore rockfish (Sebastes Spp.) populations with length frequency data. Ecol Appl 16:977–986CrossRefPubMedGoogle Scholar
  64. O’Farrell MR, Botsford LW (2006b) The fisheries management implications of maternal-age-depedent larval survival. Can J Fish Aquat Sci 63:2249–2258CrossRefGoogle Scholar
  65. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935CrossRefPubMedGoogle Scholar
  66. Olsen EM, Lilly GR, Heino M, Morgan MJ, Brattey J, Dieckmann U (2005) Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 62:811–823CrossRefGoogle Scholar
  67. Ottersen G, Hjermann DO, Stenseth NC (2006) Changes in spawning stock structure strengthen the link between climate and recruitment in a heavily fished cod (Gadus morhua) stock. Fish Oceanogr 15:230–243CrossRefGoogle Scholar
  68. Palsboll PJ, Berube M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16CrossRefPubMedGoogle Scholar
  69. Pikitch EK, Santora C, Babcock EA, Bakun A, Bonfil R, Conover DO, Dayton P, Doukakis P, Fluharty D, Heneman B, Houde ED, Link J, Livingston PA, Mangel M, McAllister MK, Pope J, Sainsbury KJ (2004) Ecosystem-based fishery management. Science 305:346–347CrossRefPubMedGoogle Scholar
  70. Rhodes KL, Sadovy Y (2002) Temporal and spatial trends in spawning aggregations of camouflage grouper, Epinephelus polyphekadion, in Pohnpei, Micronesia. Environ Biol Fish 63:27–39CrossRefGoogle Scholar
  71. Ricker WE (1954) Stock and recruitment. J Fish Res Board Can 11:559–623Google Scholar
  72. Roberts CM, Bohnsack JA, Gell F, Hawkins JP, Goodridge R (2001) Effects of marine reserves on adjacent fisheries. Science 294:1920–1923CrossRefPubMedGoogle Scholar
  73. Rochet M-J (1998) Short-term effects of fishing on life history traits of fishes. ICES J Mar Sci 55:371–391CrossRefGoogle Scholar
  74. Rochet M-J, Trenkel VM (2003) Which community indicators can measure the impact of fishing? A review and proposals. Can J Fish Aquat Sci 60:86–99CrossRefGoogle Scholar
  75. Ruttenberg BI, Haupt AJ, Chiriboga AI, Warner RR (2005) Patterns, causes and consequences of regional variation in the ecology and life history of a reef fish. Oecologia 145:394–403CrossRefPubMedGoogle Scholar
  76. Sadovy Y, Rosario A, Roman A (1994) Reproduction in an aggregating grouper, the red hind, Epinephelus guttatus. Environ Biol Fish 41:269–286Google Scholar
  77. Salvanes AGV, Stockley BM (1996) Spatial variation of growth and gonadal developments of Maurolicus muelleri in the Norwegian Sea and in a Norwegian fjord. Mar Biol 126:321–332CrossRefGoogle Scholar
  78. Scheffer M, Carpenter S, Foley JA, Folkes C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596CrossRefPubMedGoogle Scholar
  79. Scott B, Marteinsdottir G, Wright P (1999) Potential effects of maternal factors on spawning stock–recruitment relationships under varying fishing pressure. Can J Fish Aquat Sci 56:1882–1890CrossRefGoogle Scholar
  80. Scott BE, Marteinsdottir G, Begg GA, Wright PJ, Kjesbu OS (2006) Effects of population size/age structure, condition and temporal dynamics of spawning on reproductive output in Atlantic cod (Gadus morhua). Ecol Modell 191:383–415CrossRefGoogle Scholar
  81. Stokes TK, Blythe SP (1991) Size-selective harvesting and age-at-maturity II, real populations and management options: the exploitation of evolving resources. Lect Notes Biomath 99:232–247Google Scholar
  82. Stokes TK, McGlade JM, Law R (eds) (1993) The exploitation of evolving resources. Springer-Verlag, BerlinGoogle Scholar
  83. Svedang H, Righton D, Jonsson P (2007) Migratory behaviour of Atlantic cod Gadus morhua: natal homing is the prime stock-separating mechanism. Mar Ecol Prog Ser 345:1–12CrossRefGoogle Scholar
  84. Swain DP, Morin R (1996) Relationships between geographic distribution and abundance of American plaice (Hippoglossoides platessoides) in the southern Gulf of St. Lawrence. Can J Fish Aquat Sci 53:106–119CrossRefGoogle Scholar
  85. Swain DP, Sinclair AF (1994) Fish distribution and catchability: what is the appropriate measure of distribution? Can J Fish Aquat Sci 51:1046–1054CrossRefGoogle Scholar
  86. Velikanov AY (2002) Spatial differences in reproduction of capelin (Mallotus villosus socialis) in the coastal waters of Sakhalin. ICES J Mar Sci 59:1011–1017CrossRefGoogle Scholar
  87. Venturelli PA, Shuter BJ, Murphy CA (2009) Evidence for harvest-induced maternal influences on the reproductive rates of fish populations. Proc R Soc B Biol Sci 276:919–924CrossRefGoogle Scholar
  88. Wright PJ, Galley E, Gibb IM, Neat FC (2006) Fidelity of adult cod to spawning grounds in Scottish waters. Fish Res 77:148–158CrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  • Chih-hao Hsieh
    • 1
    Email author
  • Atsushi Yamauchi
    • 2
    • 3
  • Takefumi Nakazawa
    • 1
    • 2
  • Wei-Fen Wang
    • 1
  1. 1.Institute of Oceanography and Institute of Evolutionary BiologyNational Taiwan UniversityTaipeiTaiwan
  2. 2.Center for Ecological ResearchKyoto UniversityOtsuJapan
  3. 3.PRESTOJapan Science and Technology AgencyKawaguchiJapan

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